Research Studies
Study Tracker
Bacterial Cytochrome P450 Involvement in the Biodegradation of Fluorinated Pyrethroids.
| Journal of Xenobiotics | Khan MF, Liao J, Liu Z, Chugh G. | 15(2):58.
pesticides Other
View PDF

Abstract

Fluorinated pyrethroids, such as cyfluthrin and cyhalothrin, are more effective insecticides due to their enhanced stability and lipophilicity. However, they pose greater risks to non-target organisms. Their persistence in the environment and accumulation in tissues can lead to increased toxicity and ecological concerns. This study investigates the biodegradation of the fluorinated pyrethroids B-cyfluthrin (BCF) and A-cyhalothrin (LCH) using a newly isolated Bacillus sp. MFK14 from a garden soil microbial consortium. Initial screening using 19F NMR analysis showed that the microbial consortium degraded both pyrethroids, leading to the isolation of Bacillus sp. MFK14. Subsequent GC-MS analysis revealed various degradation intermediates in both pyrethroids after incubation with Bacillus sp. MFK14. Notably, Bacillus sp. MFK14 completely degraded B-cyfluthrin and A-cyhalothrin within 48 h at 30 °C. Fluoride ions from B-cyfluthrin and trifluoroacetic acid (TFA) from A-cyhalothrin were detected as the end-products by 19F NMR analysis of the aqueous fraction. The pathway of the degradation was proposed for both the pyrethroids indicating shared biodegradation pathways despite different fluorinations. Inhibition studies with 1-ABT suggested the involvement of bacterial cytochrome P450 (CYP) enzymes in their biodegradation. The CYPome of Bacillus sp. MFK14 includes 23 CYP variants that showed significant sequence similarity to known bacterial CYPs, suggesting potential roles in pyrethroid biodegradation and environmental persistence. These findings highlight the potential for bioremediation of fluorinated pesticides, offering an environmentally sustainable approach to mitigate their ecological impact.

Graphical Abstract

1. Introduction

Excessive pesticide use in agriculture adversely impacts insects, wildlife, aquatic life, plants, and human health. Among these pesticides, pyrethroids are a potent class of synthetic insecticides that effectively target a wide array of agricultural pests, mosquitoes, and flies by disrupting their nervous systems, leading to paralysis and death [1]. Compared to other insecticides, pyrethroids exhibit relatively mild toxicity to humans and mammals. However, fluorination of pyrethroids enhances their properties by increasing lipophilicity, stability, and binding affinity to biological targets, which improves their insecticidal efficacy but also heightens toxicity to non-target organisms, including humans and animals [2]. Notably, fluorinated pyrethroids—such as transfluthrin, tefluthrin, flumethrin, cyhalothrin, cyfluthrin, bifenthrin, and fluvalinate penetrate membranes more effectively, persist longer in the environment, and accumulate in biological tissues, leading to increased neurotoxicity, metabolic resistance, and potential endocrine disruption [2]. For instance, Martínez et al. investigated cyfluthrin-induced neurotoxicity in humans, revealing that it led to significant increases in ROS, lipid peroxides, and nitric oxide, along with altered gene expression related to apoptosis and inflammation due to induced oxidative stress [3]. Numerous other studies have reported their high toxicity to aquatic organisms and the adverse effects of long-term exposure on human semen quality [4,5]. Due to their environmental persistence, pyrethroids are widely detected in soil, water, and air, impacting various ecosystems and raising significant health and environmental concerns.

Microbial biodegradation has emerged as a potential strategy for mitigating pyrethroid contamination, particularly given the resistance of these compounds to metabolic detoxification pathways. Various studies have demonstrated that bacteria such as Pseudomonas aeruginosa, Bacillus licheniformis, and Bacillus subtilis, as well as fungi like Aspergillus niger, Cunninghamella elegans, and Fusarium proliferatum, can effectively degrade pyrethroid residues in water and soil [6]. For instance, Li et al. reported that a novel soil bacterial consortium effectively degraded B-cyfluthrin, with different bacterial genera like Enterobacter, Microbacterium, Ochrobactrum, and Pseudomonas playing key roles at successive stages of the degradation process [7]. In bacteria such as Bacillus subtilis BSF01, Bacillus licheniformis B-1, and Aspergillus niger YAT, pyrethroids are initially hydrolysed by carboxylesterase or pyrethroid hydrolase, which cleaves the main ester bond linking the cyclopropane and aromatic moieties [8,9]. Similarly, in fungi like Cunninghamella elegans, cytochrome P450 enzymes (CYP5208A3) mediate cleavage of the central ester bonds [10,11].

Cytochrome P450 enzymes (CYP) play a crucial role in the biodegradation of various environmental pollutants by catalysing oxidation reactions that enhance the solubility and breakdown of complex organic compounds, including pesticides, hydrocarbons, and pharmaceuticals [12]. While the role of fungal cytochrome P450 enzymes in pyrethroid degradation is well established, there are limited reports on bacterial cytochrome P450 enzymes in this process. Li et al. highlighted the significance of these enzymes in the late-stage metabolism of B-cyfluthrin, particularly in the breakdown of benzoate intermediates. However, the involvement of bacterial cytochrome P450 enzymes in the initial cleavage of pyrethroid ester bonds remains largely unreported [7]. Further degradation generally involves oxidation and cleavage of pyrethroid aromatic rings facilitated by enzymes such as phenol hydrolases, monooxygenases, and dioxygenases [13].

In addition, fluorinated xenobiotic compounds, including pesticides, pose a significant challenge to biodegradation due to the stability of the carbon–fluorine (C-F) bond—the strongest in organic chemistry. Microbial enzymes have not naturally evolved to efficiently cleave C-F bonds, making these compounds persist in the environment and complicating their microbial degradation [12].

In this study, we explore the biodegradation of the fluorinated pyrethroids B-cyfluthrin and A-cyhalothrin using microbial isolates from garden soil. We identify bacterial strains capable of metabolising these compounds and examine the degradation pathways involved. The identification of degradation intermediates, including fluoride ions and trifluoroacetic acid, was achieved using GC-MS and 19F NMR analysis. Furthermore, inhibition studies confirmed the involvement of cytochrome P450 enzymes in multiple steps of the biodegradation process. These findings highlight the potential for an environmentally sustainable approach to mitigate the ecological impact of fluorinated pesticides. By elucidating the microbial degradation pathways and identifying key enzymatic players, this study paves the way for developing bioremediation strategies that harness naturally occurring bacteria to detoxify contaminated environments. Such approaches could reduce pesticide accumulation in soil and water, minimising harmful effects on ecosystems while promoting sustainable agricultural and environmental management practices.

4. Discussion

The use of pyrethroids in agriculture practices for pest control leads to environmental pollution, negatively impacting human health and reducing soil microbial populations, which diminishes soil fertility [17]. Some soil bacteria can tolerate these harmful metabolites, evolving mechanisms to degrade pyrethroids [18]. In this study, we utilised a bacterial consortium isolated from garden soil to degrade the fluorinated pyrethroids B-cyfluthrin and A-cyhalothrin. Similar studies, such as Birolli et al., Liu et al., and Zhang et al., have demonstrated the degradation of various pyrethroids using bacterial consortia from different environments [19,20,21]. Our study found that newly isolated Bacillus sp. MFK14 from garden soil completely degraded the B-cyfluthrin and A-cyhalothrin within 48 h, producing 13 metabolites in each pesticide. In comparison, previous research reported that Bacillus subtilis BSF01 degraded 89.4% of 50 mg/L B-cypermethrin in 7 days [9], Brevibacterium aureum DG-12 achieved 88.6% degradation of 50 mg/L B-cyfluthrin within 5 days [22], and Bacillus thuringiensis ZS-19 completely degraded 100 mg/L of ?-cyhalothrin in 72 h [23]. The degradation efficiency of A-cyhalothrin and B-cyfluthrin in bacteria and fungi is summarised in Table 2, comparing the findings of this study with previously reported microbial strains.

Table 2. Comparison of B-cyfluthrin and A-cyhalothrin degradation by different microorganisms.

Esterases play a vital role in pyrethroid degradation by cleaving the primary ester bonds in these compounds [29]. A carboxylesterase from Bacillus cereus BCC01, which functioned at pH 8 and 30 °C, was characterised for its pyrethroid-degrading activity [30]. Similarly, a cypermethrin-degrading esterase from Bacillus subtilis was most effective at pH 7.0 and 32 °C [31]. However, beyond esterase activity, our study also demonstrated that the degradation of B-cyfluthrin and A-cyhalothrin involved cytochrome P450 (CYP)-mediated cleavage of ester bonds in Bacillus sp. MFK14. This was confirmed using 1-ABT, a CYP inhibitor, which showed that B-cyfluthrin was transformed into M4 and M11, while A-cyhalothrin was converted to N11 and N2 through CYP-mediated biotransformation. Khan and Murphy previously identified similar ester bond hydrolysis in transfluthrin and B-cyfluthrin by Cunninghamella spp. (C. elegans, C. blakesleeana, and C. echinulata), attributing this activity to cytochrome P450s (CYPs) [10]. Further research revealed that CYP5208A3 and CYP5313D1, along with their redox partner CYP reductase (CPR_C) from C. elegans, were involved in the oxidative ester cleavage of the transfluthrin pyrethroid [10]. Additionally, Hedges et al. demonstrated significant variability in the activity of recombinant human CYPs across different pyrethroids (including A-cyhalothrin, bifenthrin, and B-cyfluthrin), with CYP2C19 showing the highest effectiveness [32]. Our study further revealed that CYPs in Bacillus sp. MFK14 not only cleaved ester bonds but also participated in the transformation of various metabolites in B-cyfluthrin and A-cyhalothrin biodegradation. Specifically, B-cyfluthrin was transformed through M4 to M7, M2 to M7, and M10 to M12, while A-cyhalothrin was converted from N2 to N12, N1 to N12, and N7 to N10. These conversions were supported by CYP inhibition experiments (Figure 6C). In silico analysis of the CYPome in Bacillus sp. MFK14 genome revealed a significant number of CYP genes (23 variants), indicating a high potential for CYPs to participate in ester hydrolysis, as well as monooxygenation, defluorination, and other reactions during pyrethroid biodegradation.

The presence of fluoride ions in B-cyfluthrin and trifluoroacetic acid in A-cyhalothrin following 48 h of incubation with Bacillus sp. MFK14 was confirmed by 19F-NMR analysis of the aqueous fraction. The release of fluoride ions likely occurred during the conversion of 4-fluorobenzene-1,3-diol (M3) to hydroxyquinol (M5) in B-cyfluthrin biodegradation, potentially catalysed by cytochrome P450s (CYPs), as previously described by Harkey et al. in the CYP-mediated oxidative defluorination of 4-fluorophenol to hydroquinone [33]. Similarly, Li et al. observed defluorinated metabolites in the bacterial degradation of B-cyfluthrin [7].

Dechlorination of the 2,2-dichlorovinyl group in B-cyfluthrin (conversion from M7 to M9) and the 2-chloro-3,3,3-trifluoroprop-1-en-1-yl group in A-cyhalothrin (conversion from N12 to N9) was rare, with limited reports documenting these dechlorinated metabolites. For example, Birolli et al. demonstrated that a Bacillus sp. CSA-1 consortium of 10 bacterial strains achieved rapid CYP-mediated biodegradation of cypermethrin, identifying dechlorinated metabolites via LC-MS/MS analysis [19]. Additionally, Li et al. identified a dechlorinated metabolite, (2,2,3,3-tetramethyl-cyclopropyl)-methanol, resulting from the removal of terminal chlorines during CYP-mediated B-cyfluthrin degradation by a bacterial consortium [7]. Zhang et al. reviewed the dechlorination of 2,2-dichlorovinyl groups in dichlorvos by various microorganisms, including Pseudomonas, Bacillus, Fusarium, Aspergillus, and Trichoderma. Consequently, the dechlorination of the 2-chloro-3,3,3-trifluoroprop-1-en-1-yl group in A-cyhalothrin may have resulted in the release of trifluoroacetic acid, as identified in our 19F-NMR analysis [34].

In addition to CYPs, the degradation processes for both pyrethroids involved a possible range of enzymes, including hydrolases, dioxygenases, etc. Earlier work by Schmidt et al. described the nonspecific attack of dioxygenase on halodiphenyl ethers, leading to the formation of halophenols during biodegradation by Sphingomonas sp. strain SS3 [35]. This mechanism is commonly observed in both bacterial and fungal degradation [36,37]. In our study, Bacillus sp. MFK14 exhibited a similar diphenyl ether moiety degradation pattern in both B-cyfluthrin and A-cyhalothrin. Following diphenyl ether cleavage, the phenolic metabolites hydroquinone (M1/N3) at 10.16 min, resorcinol (N4) at 10.50 min, and hydroxyquinol (M5/N6) at 13.27 min were identified by comparing their retention times and mass spectra with those of authentic standards. These findings provide strong evidence for the production of these phenolic metabolites during the biodegradation of B-cyfluthrin and A-cyhalothrin by Bacillus sp. MFK14.

The genome analysis of Bacillus sp. MFK14 also revealed the presence of catechol-2,3-dioxygenase with high sequence identity (99%) to Bacillus subtilis strain 168 catechol-2,3-dioxygenase (Protein ID: P54721). This supported the observed ring cleavage from hydroxyquinol (M5/N6) to 4-hydroxy-6-oxohexa-2,4-dienoic acid (M6/N8) in both pesticides, which was subsequently catabolised through the TCA cycle. In summary, the proposed biodegradation pathways for ?-cyfluthrin and ?-cyhalothrin by Bacillus sp. MFK14 illustrated the complex interplay of various enzymes in breaking down these fluorinated pyrethroids. Understanding these pathways enhanced our knowledge of microbial degradation mechanisms and could have informed strategies for environmental remediation.

5. Conclusions

This study highlighted the crucial role of cytochrome P450 enzymes in the biodegradation of fluorinated pyrethroids by Bacillus sp. MFK14, a newly isolated strain from garden soil. The strain effectively degraded B-cyfluthrin and A-cyhalothrin, releasing fluoride ions and trifluoroacetic acid (TFA), demonstrating the potential of microbial bioremediation to mitigate the environmental impact of these persistent insecticides. Notably, Bacillus sp. MFK14 completely degraded both ?-cyfluthrin and ?-cyhalothrin within 48 h at 30 °C, showcasing its efficiency in degrading these hazardous compounds. The findings also revealed that, despite differing fluorinations, B-cyfluthrin and A-cyhalothrin shared degradation pathways, showcasing the adaptability and specificity of bacterial CYP enzymes in breaking down complex compounds. Inhibition studies with 1-ABT further confirm the involvement of CYP enzymes in this process, while genomic analysis of Bacillus sp. MFK14’s CYPome showed significant sequence similarity with known bacterial CYPs, highlighting the evolutionary conservation and functional importance of these enzymes.

6. Future Perspectives

Microbial degradation offers an eco-friendly, cost-effective solution for pesticide, herbicide, and insecticide remediation, with advantages over traditional methods by breaking down pollutants into less toxic forms. It can be applied in situ, reducing environmental persistence and preserving soil and water quality. However, its efficiency can vary with environmental conditions, and challenges such as toxic intermediates and slow microbial adaptation to synthetic pollutants exist. Genetic engineering and optimising microbial consortia could improve the process and enhance its sustainability. In line with these considerations, the environmental challenges posed by fluorinated pyrethroids make this research a promising foundation for developing biotechnological applications aimed at reducing their persistence and toxicity. Future studies should focus on the genetic engineering of Bacillus sp. MFK14 and heterologous expression of predicted CYPs to enhance degradation efficiency. Moreover, investigating the interaction of these bacterial CYPs with other classes of persistent organic pollutants could broaden the scope of bioremediation strategies, ultimately contributing to more sustainable agricultural practices.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/jox15020058/s1: Figure S1: GC-MS analysis of standards: (A) ?-cyfluthrin, and (B) ?-cyhalothrin; Figure S2: Mass spectrum of metabolite M1 or N3 (tR = 10.16 min; M+ = 254); Figure S3: Mass spectrum of metabolite M2 (tR = 10.91 min; M+ = 192); Figure S4: Mass spectrum of metabolite M3 (tR = 11.36 min; M+ = 272 (257+15)); Figure S5: Mass spectrum of metabolite M4 (tR = 11.59 min; M+ = 280 (265+15)); Figure S6: Mass spectrum of metabolite M5 or N6 (tR = 13.27 min; M+ = 342); Figure S7: Mass spectrum of metabolite M6 or N8 (tR = 14.46 min; M+ = 286); Figure S8: Mass spectrum of metabolite M7 (tR = 14.69 min; M+ = 368 (353+15)); Figure S9: Mass spectrum of metabolite M8 (tR = 15.14 min; M+ = 300); Figure S10: Mass spectrum of metabolite M9 or N9 (tR = 15.59 min; M+ = 302); Figure S11: Mass spectrum of metabolite M10 (tR = 15.85 min; M+ = 290); Figure S12: Mass spectrum of metabolite M11 (tR = 16.19 min; M+ = 315); Figure S13: Mass spectrum of metabolite M12 (tR = 16.59 min; M+ = 304); Figure S14: Mass spectrum of metabolite M13 (tR = 19.66 min; M+ = 392); Figure S15: Mass spectrum of metabolite N1 (tR = 8.33 min; M+ = 226); Figure S16: Mass spectrum of metabolite N2 (tR = 9.15 min; M+ = 314 (299+15)); Figure S17: Mass spectrum of metabolite N4 (tR = 10.50 min; M+ = 254); Figure S18: Mass spectrum of metabolite N5 (tR = 12.83 min; M+ = 282); Figure S19: Mass spectrum of metabolite N7 (tR = 13.53 min; M+ = 272); Figure S20: Mass spectrum of metabolite N10 (tR = 16.88 min; M+ = 286); Figure S21: Mass spectrum of metabolite N11 (tR = 18.88 min; M+ = 297); Figure S22: Mass spectrum of metabolite N12 (tR = 19.03 min; M+ = 402 (387+15)); Figure S23: Mass spectrum of metabolite N13 (tR = 20.70 min; M+ = 374); Figure S24: GC-MS analysis of standards: (A) resorcinol, (B) hydroquinone, and (C) hydroxyquinol; Figure S25: 19F-NMR analysis confirmed the presence of (A) fluoride ion in B-cyfluthrin, and (B) trifluoroacetic acid in A-cyhalothrin after 48 h incubation with Bacillus sp. MFK14; Table S1: Putative CYP sequences were extracted from the newly sequenced genome of Bacillus sp. MFK14.

Funding

The UCD Internal supported this research financially (Award number: 82930-NP).

Data Availability Statement

Data will be made available on request.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:

1-ABT 1-aminobenzotriazole
19F NMR 19F nuclear magnetic resonance spectroscopy
BCF ?-cyfluthrin
LCH ?-cyhalothrin
CYP Cytochrome P450
GC-MS Gas chromatography-mass spectrometry
PBS Phosphate-buffered saline
p-NPA p-Nitrophenyl acetate
PMSF Phenylmethylsulfonyl fluoride
TFA Trifluoroacetic acid
TSB Tryptone soya broth
TSA Tryptone soya agar
References

  1. Asem, D.; Kumari, M.; Singh, L.R.; Bhushan, M. Pesticides: Pollution, risks, and abatement measures. In Emerging Aquatic Contaminants, 2nd ed.; Elsevier: Amsterdam, The Netherlands, 2023; pp. 307–326. [Google Scholar]
  2. Galadima, M.; Singh, S.; Pawar, A.; Khasnabis, S.; Dhanjal, D.S.; Anil, A.G.; Rai, P.; Ramamurthy, P.C.; Singh, J. Toxicity, microbial degradation and analytical detection of pyrethroids: A review. Environ. Adv. 2021, 5, 100105. [Google Scholar] [CrossRef]
  3. Martínez, M.A.; Rodríguez, J.L.; Lopez-Torres, B.; Martínez, M.; Martínez-Larrañaga, M.R.; Anadón, A.; Ares, I. Oxidative stress and related gene expression effects of cyfluthrin in human neuroblastoma SH-SY5Y cells: Protective effect of melatonin. Environ. Res. 2019, 177, 108579. [Google Scholar] [CrossRef] [PubMed]
  4. Ham, J.; You, S.; Lim, W.; Song, G. Bifenthrin impairs the functions of Leydig and Sertoli cells in mice via mitochondrion-endoplasmic reticulum dysregulation. Environ. Pollut. 2020, 266, 115174. [Google Scholar] [CrossRef] [PubMed]
  5. Wang, R.; Wang, F.; Lu, Y.; Zhang, S.; Cai, M.; Guo, D.; Zheng, H. Spatial distribution and risk assessment of pyrethroid insecticides in surface waters of East China Sea estuaries. Environ. Pollut. 2024, 344, 123302. [Google Scholar] [CrossRef]
  6. Huang, Y.; Chen, S. Pyrethroid-degrading microorganisms and their potential application for the bioremediation of contaminated environments. In Enzymes for Pollutant Degradation; Springer Nature: Singapore, 2022; pp. 119–137. [Google Scholar]
  7. Li, H.; Ma, Y.; Yao, T.; Ma, L.; Zhang, J.; Li, C. Biodegradation pathway and detoxification of ?-cyfluthrin by the bacterial consortium and its bacterial community structure. J. Agric. Food Chem. 2022, 70, 7626–7635. [Google Scholar] [CrossRef]
  8. Deng, W.; Lin, D.; Yao, K.; Yuan, H.; Wang, Z.; Li, J.; Zou, L.; Han, X.; Zhou, K.; He, L.; et al. Characterization of a novel ?-cypermethrin-degrading Aspergillus niger YAT strain and the biochemical degradation pathway of ?-cypermethrin. Appl. Microbiol. Biotechnol. 2015, 99, 8187–8198. [Google Scholar] [CrossRef]
  9. Xiao, Y.; Chen, S.; Gao, Y.; Hu, W.; Hu, M.; Zhong, G. Isolation of a novel beta-cypermethrin degrading strain Bacillus subtilis BSF01 and its biodegradation pathway. Appl. Microbiol. Biotechnol. 2015, 99, 2849–2859. [Google Scholar] [CrossRef]
  10. Khan, M.F.; Murphy, C.D. Cunninghamella spp. produce mammalian-equivalent metabolites from fluorinated pyrethroid pesticides. AMB Express 2021, 11, 101. [Google Scholar] [CrossRef]
  11. Khan, M.F.; Murphy, C.D. Cytochrome P450 5208A3 is a promiscuous xenobiotic biotransforming enzyme in Cunninghamella elegans. Enzyme Microb. Technol. 2022, 161, 110102. [Google Scholar] [CrossRef]
  12. Khan, M.F.; Hof, C.; Niemcova, P.; Murphy, C.D. Biotransformation of fluorinated drugs and xenobiotics by the model fungus Cunninghamella elegans. Methods Enzymol. 2024, 696, 251–285. [Google Scholar]
  13. Tang, J.; Liu, B.; Chen, T.T.; Yao, K.; Zeng, L.; Zeng, C.Y.; Zhang, Q. Screening of a beta-cypermethrin-degrading bacterial strain Brevibacillus parabrevis BCP-09 and its biochemical degradation pathway. Biodegradation 2018, 29, 525–541. [Google Scholar] [CrossRef] [PubMed]
  14. Khan, M.F.; Chowdhary, S.; Koksch, B.; Murphy, C.D. Biodegradation of amphipathic fluorinated peptides reveals a new bacterial defluorinating activity and a new source of natural organofluorine compounds. Environ. Sci. Technol. 2023, 57, 9762–9772. [Google Scholar] [CrossRef] [PubMed]
  15. Khan, M.F.; Murphy, C.D. Bacterial degradation of the anti-depressant drug fluoxetine produces trifluoroacetic acid and fluoride ion. Appl. Microbiol. Biotechnol. 2021, 105, 9359–9369. [Google Scholar] [CrossRef] [PubMed]
  16. Hof, C.; Khan, M.F.; Murphy, C.D. Endogenous production of 2-phenylethanol by Cunninghamella echinulata inhibits biofilm growth of the fungus. Fungal Biol. 2023, 127, 1384–1388. [Google Scholar] [CrossRef]
  17. Singh, S.; Mukherjee, A.; Jaiswal, D.K.; de Araujo Pereira, A.P.; Prasad, R.; Sharma, M.; Kuhad, R.C.; Shukla, A.C.; Verma, J.P. Advances and future prospects of pyrethroids: Toxicity and microbial degradation. Sci. Total Environ. 2022, 829, 154561. [Google Scholar] [CrossRef]
  18. Cyco?, M.; Piotrowska-Seget, Z. Pyrethroid-degrading microorganisms and their potential for the bioremediation of contaminated soils: A review. Front. Microbiol. 2016, 7, 1463. [Google Scholar] [CrossRef]
  19. Birolli, W.G.; da Silva, B.F.; Rodrigues Filho, E. Biodegradation of the pyrethroid cypermethrin by bacterial consortia collected from orange crops. Environ. Res. 2022, 215, 114388. [Google Scholar] [CrossRef]
  20. Liu, J.; Ding, Y.; Ma, L.; Gao, G.; Wang, Y. Combination of biochar and immobilized bacteria in cypermethrin-contaminated soil remediation. Int. Biodeter. Biodegr. 2017, 120, 15–20. [Google Scholar] [CrossRef]
  21. Zhang, H.; Zhang, Y.; Hou, Z.; Wang, X.; Wang, J.; Lu, Z.; Zhao, X.; Sun, F.; Pan, H. Biodegradation potential of deltamethrin by the Bacillus cereus strain Y1 in both culture and contaminated soil. Int. Biodeter. Biodegr. 2016, 106, 53–59. [Google Scholar] [CrossRef]
  22. Chen, S.; Dong, Y.H.; Chang, C.; Deng, Y.; Zhang, X.F.; Zhong, G.; Song, H.; Hu, M.; Zhang, L.H. Characterization of a novel cyfluthrin-degrading bacterial strain Brevibacterium aureum and its biochemical degradation pathway. Bioresour. Technol. 2013, 132, 16–23. [Google Scholar] [CrossRef]
  23. Chen, S.; Deng, Y.; Chang, C.; Lee, J.; Cheng, Y.; Cui, Z.; Zhou, J.; He, F.; Hu, M.; Zhang, L.H. Pathway and kinetics of cyhalothrin biodegradation by Bacillus thuringiensis strain ZS-19. Sci. Rep. 2015, 5, 8784. [Google Scholar] [CrossRef] [PubMed]
  24. Wang, T.; Hu, C.; Zhang, R.; Sun, A.; Li, D.; Shi, X. Mechanism study of cyfluthrin biodegradation by Photobacterium ganghwense with comparative metabolomics. Appl. Microbiol. Biotechnol. 2019, 103, 473–488. [Google Scholar] [CrossRef] [PubMed]
  25. Hu, G.P.; Zhao, Y.; Song, F.Q.; Liu, B.; Vasseur, L.; Douglas, C.; You, M.S. Isolation, identification and cyfluthrin-degrading potential of a novel Lysinibacillus sphaericus strain, FLQ-11-1. Res. Microbiol. 2014, 165, 110–118. [Google Scholar] [CrossRef]
  26. Tian, J.W.; Long, X.F.; Zhang, S.; Qin, Q.M.; Gan, L.Z.; Tian, Y.Q. Screening cyhalothrin degradation strains from locust epiphytic bacteria and studying Paracoccus acridae SCU-M53 cyhalothrin degradation process. Environ. Sci. Pollut. Res. 2018, 25, 11505–11515. [Google Scholar] [CrossRef]
  27. Palmer-Brown, W.; de Melo Souza, P.L.; Murphy, C.D. Cyhalothrin biodegradation in Cunninghamella elegans. Environ. Sci. Pollut. Res. Int. 2019, 26, 1414–1421. [Google Scholar] [CrossRef]
  28. Birolli, W.G.; Vacondio, B.; Alvarenga, N.; Seleghim, M.H.R.; Porto, A.L.M. Enantioselective biodegradation of the pyrethroid (+/)-lambda-cyhalothrin by marine-derived fungi. Chemosphere 2018, 197, 651–660. [Google Scholar] [CrossRef]
  29. Bhatt, P.; Bhatt, K.; Huang, Y.; Lin, Z.; Chen, S. Esterase is a powerful tool for the biodegradation of pyrethroid insecticides. Chemosphere 2020, 244, 125507. [Google Scholar] [CrossRef]
  30. Hu, W.; Lu, Q.; Zhong, G.; Hu, M.; Yi, X. Biodegradation of pyrethroids by a hydrolyzing carboxylesterase EstA from Bacillus cereus BCC01. Appl. Sci. 2019, 9, 477. [Google Scholar] [CrossRef]
  31. Gangola, S.; Sharma, A.; Bhatt, P.; Khati, P.; Chaudhary, P. Presence of esterase and laccase in Bacillus subtilis facilitates biodegradation and detoxification of cypermethrin. Sci. Rep. 2018, 8, 12755. [Google Scholar] [CrossRef]
  32. Hedges, L.; Brown, S.; MacLeod, A.K.; Moreau, M.; Yoon, M.; Creek, M.R.; Osimitz, T.G.; Lake, B.G. Metabolism of bifenthrin, ?-cyfluthrin, ?-cyhalothrin, cyphenothrin and esfenvalerate by rat and human cytochrome P450 and carboxylesterase enzymes. Xenobiotica 2020, 50, 1434–1442. [Google Scholar] [CrossRef]
  33. Harkey, A.; Kim, H.J.; Kandagatla, S.; Raner, G.M. Defluorination of 4-fluorophenol by cytochrome P450BM3-F87G: Activation by long chain fatty aldehydes. Biotechnol. Lett. 2012, 34, 1725–1731. [Google Scholar] [CrossRef] [PubMed]
  34. Zhang, Y.; Zhang, W.; Li, J.; Pang, S.; Mishra, S.; Bhatt, P.; Zeng, D.; Chen, S. Emerging technologies for degradation of dichlorvos: A review. Int. J. Environ. Res. Public Health 2021, 18, 5789. [Google Scholar] [CrossRef] [PubMed]
  35. Schmidt, S.; Wittich, R.M.; Erdmann, D.; Wilkes, H.; Francke, W.; Fortnagel, P. Biodegradation of diphenyl ether and its monohalogenated derivatives by Sphingomonas sp. strain SS3. Appl. Environ. Microbiol. 1992, 58, 2744–2750. [Google Scholar] [CrossRef]
  36. Gu, C.; Jin, Z.; Fan, X.; Ti, Q.; Yang, X.; Sun, C.; Jiang, X. Comparative evaluation and prioritization of key influences on biodegradation of 2, 2?, 4, 4?-tetrabrominated diphenyl ether by bacterial isolate B. xenovorans LB400. J. Environ. Manag. 2023, 331, 117320. [Google Scholar] [CrossRef]
  37. Hundt, K.; Jonas, U.; Hammer, E.; Schauer, F. Transformation of diphenyl ethers by Trametes versicolor and characterization of ring cleavage products. Biodegradation 1999, 10, 279–286. [Google Scholar] [CrossRef]

FULL-TEXT STUDY ONLINE AT
https://www.mdpi.com/2039-4713/15/2/58